{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,6]],"date-time":"2026-03-06T11:07:46Z","timestamp":1772795266630,"version":"3.50.1"},"reference-count":69,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2022,3,31]],"date-time":"2022-03-31T00:00:00Z","timestamp":1648684800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["CRC 1080, C02"],"award-info":[{"award-number":["CRC 1080, C02"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Posttraumatic epilepsy (PTE) is a major public health concern and strongly contributes to human epilepsy cases worldwide. However, an effective treatment and prevention remains a matter of intense research. The present study provides new insights into the gamma aminobutyric acid A (GABAA)-stabilizing protein ubiquilin-1 (ubqln1) and its regulation in mouse models of traumatic brain injury (TBI) and in vitro epilepsy. We performed label-free quantification on isolated cortical GABAergic interneurons from GAD67-GFP mice that received unilateral TBI and discovered reduced expression of ubqln1 24 h post-TBI. To investigate the link between this regulation and the development of epileptiform activity, we further studied ubqln1 expression in hippocampal and cortical slices. Epileptiform events were evoked pharmacologically in acute brain slices by administration of picrotoxin (PTX, 50 \u03bcM) and kainic acid (KA, 500 nM) and recorded in the hippocampal CA1 subfield using Multi-electrode Arrays (MEA). Interestingly, quantitative Western blots revealed significant decreases in ubqln1 expression 1\u20137 h after seizure induction that could be restored by application of the non-selective monoamine oxidase inhibitor nialamide (NM, 10 \u03bcM). In picrotoxin-dependent dose\u2013response relationships, NM administration alleviated the frequency and peak amplitude of seizure-like events (SLEs). These findings indicate a role of the monoamine transmitter systems and ubqln1 for cortical network activity during posttraumatic epileptogenesis.<\/jats:p>","DOI":"10.3390\/ijms23073902","type":"journal-article","created":{"date-parts":[[2022,3,31]],"date-time":"2022-03-31T21:34:29Z","timestamp":1648762469000},"page":"3902","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["GABAA Receptor-Stabilizing Protein Ubqln1 Affects Hyperexcitability and Epileptogenesis after Traumatic Brain Injury and in a Model of In Vitro Epilepsy in Mice"],"prefix":"10.3390","volume":"23","author":[{"given":"Tabea","family":"K\u00fcrten","sequence":"first","affiliation":[{"name":"Institute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Duesbergweg 6, 55128 Mainz, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6514-2806","authenticated-orcid":false,"given":"Natascha","family":"Ihbe","sequence":"additional","affiliation":[{"name":"Institute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Duesbergweg 6, 55128 Mainz, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Timo","family":"Ueberbach","sequence":"additional","affiliation":[{"name":"Institute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Duesbergweg 6, 55128 Mainz, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8031-6384","authenticated-orcid":false,"given":"Ute","family":"Distler","sequence":"additional","affiliation":[{"name":"Institute for Immunology, University Medical Center of the Johannes Gutenberg University Mainz, Langenbeckstra\u00dfe 1, 55131 Mainz, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Malte","family":"Sielaff","sequence":"additional","affiliation":[{"name":"Institute for Immunology, University Medical Center of the Johannes Gutenberg University Mainz, Langenbeckstra\u00dfe 1, 55131 Mainz, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3034-0017","authenticated-orcid":false,"given":"Stefan","family":"Tenzer","sequence":"additional","affiliation":[{"name":"Institute for Immunology, University Medical Center of the Johannes Gutenberg University Mainz, Langenbeckstra\u00dfe 1, 55131 Mainz, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6002-2963","authenticated-orcid":false,"given":"Thomas","family":"Mittmann","sequence":"additional","affiliation":[{"name":"Institute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Duesbergweg 6, 55128 Mainz, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,3,31]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.seizure.2015.10.002","article-title":"Traumatic brain injury and epilepsy: Underlying mechanisms leading to seizure","volume":"33","author":"Nguyen","year":"2015","journal-title":"Seizure"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"3105","DOI":"10.1007\/s00415-020-09926-w","article-title":"A review of seizures and epilepsy following traumatic brain injury","volume":"267","author":"Fordington","year":"2020","journal-title":"J. Neurol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1111\/j.1528-1167.2008.02004.x","article-title":"Epilepsy after head injury: An overview","volume":"50","author":"Lowenstein","year":"2009","journal-title":"Epilepsia"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"a022822","DOI":"10.1101\/cshperspect.a022822","article-title":"Epileptogenesis","volume":"5","author":"Lukasiuk","year":"2015","journal-title":"Cold Spring Harb. Perspect. Med."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1111\/nan.12451","article-title":"Review: Animal models of acquired epilepsy: Insights into mechanisms of human epileptogenesis","volume":"44","author":"Becker","year":"2018","journal-title":"Neuropathol. Appl. Neurobiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"9034","DOI":"10.1523\/JNEUROSCI.3507-17.2018","article-title":"Early Appearance and Spread of Fast Ripples in the Hippocampus in a Model of Cortical Traumatic Brain Injury","volume":"38","author":"Ortiz","year":"2018","journal-title":"J. Neurosci. Off. J. Soc. Neurosci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1105","DOI":"10.1016\/S0140-6736(09)60214-2","article-title":"Long-term risk of epilepsy after traumatic brain injury in children and young adults: A population-based cohort study","volume":"373","author":"Christensen","year":"2009","journal-title":"Lancet"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"527605","DOI":"10.1155\/2011\/527605","article-title":"Altered GABA signaling in early life epilepsies","volume":"2011","author":"Briggs","year":"2011","journal-title":"Neural Plast."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1007\/s11910-015-0545-1","article-title":"Glutamate and GABA imbalance following traumatic brain injury","volume":"15","author":"Guerriero","year":"2015","journal-title":"Curr. Neurol. Neurosci. Rep."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1207","DOI":"10.1042\/CS20150202","article-title":"Plic-1, a new target in repressing epileptic seizure by regulation of GABAAR function in patients and a rat model of epilepsy","volume":"129","author":"Zhang","year":"2015","journal-title":"Clin. Sci."},{"key":"ref_11","first-page":"S23","article-title":"Prolonged seizures: What are the mechanisms that predispose or cease to be protective? A review of animal data","volume":"16","year":"2014","journal-title":"Epileptic Disord. Int. Epilepsy J. Videotape"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"15073","DOI":"10.1073\/pnas.1313505110","article-title":"GABA(B) autoreceptor-mediated cell type-specific reduction of inhibition in epileptic mice","volume":"110","author":"Dugladze","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2306","DOI":"10.1093\/cercor\/bhu041","article-title":"Traumatic Brain Injury Increases Cortical Glutamate Network Activity by Compromising GABAergic Control","volume":"25","author":"Cantu","year":"2015","journal-title":"Cereb. Cortex"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"614329","DOI":"10.1155\/2011\/614329","article-title":"Functional consequences of the disturbances in the GABA-mediated inhibition induced by injuries in the cerebral cortex","volume":"2011","author":"Imbrosci","year":"2011","journal-title":"Neural Plast."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1649","DOI":"10.1007\/s00429-014-0750-8","article-title":"Neuronal mechanisms underlying transhemispheric diaschisis following focal cortical injuries","volume":"220","author":"Imbrosci","year":"2015","journal-title":"Brain Struct. Funct."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1080\/01616412.1993.11740164","article-title":"Diaschisis","volume":"15","author":"Meyer","year":"1993","journal-title":"Neurol. Res."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1097","DOI":"10.1089\/neu.2016.4575","article-title":"Acute Cortical Transhemispheric Diaschisis after Unilateral Traumatic Brain Injury","volume":"34","author":"Thal","year":"2017","journal-title":"J. Neurotrauma"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1016\/S1097-2765(00)00040-X","article-title":"The hPLIC proteins may provide a link between the ubiquitination machinery and the proteasome","volume":"6","author":"Kleijnen","year":"2000","journal-title":"Mol. Cell"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1016\/j.neuron.2011.03.024","article-title":"GABAA receptor trafficking-mediated plasticity of inhibitory synapses","volume":"70","author":"Luscher","year":"2011","journal-title":"Neuron"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1016\/S0968-0004(03)00092-6","article-title":"A potential proteasome-interacting motif within the ubiquitin-like domain of parkin and other proteins","volume":"28","author":"Upadhya","year":"2003","journal-title":"Trends Biochem. Sci."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1016\/j.febslet.2004.04.031","article-title":"Ubiquilin interacts with ubiquitylated proteins and proteasome through its ubiquitin-associated and ubiquitin-like domains","volume":"566","author":"Ko","year":"2004","journal-title":"FEBS Lett."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"73","DOI":"10.3389\/fnmol.2014.00073","article-title":"The ubiquitin proteasome system in glia and its role in neurodegenerative diseases","volume":"7","author":"Jansen","year":"2014","journal-title":"Front. Mol. Neurosci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"18538","DOI":"10.1074\/jbc.M802077200","article-title":"The ubiquitin-like protein Plic-1 enhances the membrane insertion of GABAA receptors by increasing their stability within the endoplasmic reticulum","volume":"283","author":"Saliba","year":"2008","journal-title":"J. Biol. Chem."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"908","DOI":"10.1038\/nn0901-908","article-title":"GABA(A) receptor cell surface number and subunit stability are regulated by the ubiquitin-like protein Plic-1","volume":"4","author":"Bedford","year":"2001","journal-title":"Nat. Neurosci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/j.nbd.2015.11.005","article-title":"Relationship between ubiquilin-1 and BACE1 in human Alzheimer\u2019s disease and APdE9 transgenic mouse brain and cell-based models","volume":"85","author":"Natunen","year":"2016","journal-title":"Neurobiol. Dis."},{"key":"ref_26","first-page":"18","article-title":"An emerging role for Ubiquilin 1 in regulating protein quality control system and in disease pathogenesis","volume":"8","author":"Zhang","year":"2009","journal-title":"Discov. Med."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.brainres.2014.12.008","article-title":"Signature changes in ubiquilin expression in the R6\/2 mouse model of Huntington\u2019s disease","volume":"1597","author":"Safren","year":"2015","journal-title":"Brain Res."},{"key":"ref_28","first-page":"4597","article-title":"Decreased expression of ubiquilin-1 following neonatal hypoxia-ischemic brain injury in mice","volume":"19","author":"Luo","year":"2019","journal-title":"Mol. Med. Rep."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"937","DOI":"10.1007\/s12035-019-01788-2","article-title":"Attenuation of Ischemic Stroke-Caused Brain Injury by a Monoamine Oxidase Inhibitor Involves Improved Proteostasis and Reduced Neuroinflammation","volume":"57","author":"Liu","year":"2020","journal-title":"Mol. Neurobiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1093","DOI":"10.1093\/cercor\/bhab268","article-title":"Adaptive Mechanisms of Somatostatin-Positive Interneurons after Traumatic Brain Injury through a Switch of \u03b1 Subunits in L-Type Voltage-Gated Calcium Channels","volume":"32","author":"Ihbe","year":"2022","journal-title":"Cereb. Cortex"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1038\/s41582-018-0058-z","article-title":"Neurofilaments as biomarkers in neurological disorders","volume":"14","author":"Khalil","year":"2018","journal-title":"Nat. Rev. Neurol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1364","DOI":"10.1016\/S0960-9822(01)00424-9","article-title":"Gap junction protein connexin-43 interacts directly with microtubules","volume":"11","author":"Giepmans","year":"2001","journal-title":"Curr. Biol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1065","DOI":"10.1289\/ehp.6361","article-title":"Parkinson\u2019s disease and exposure to infectious agents and pesticides and the occurrence of brain injuries: Role of neuroinflammation","volume":"111","author":"Liu","year":"2003","journal-title":"Environ. Health Perspect."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"158","DOI":"10.4161\/bioa.21791","article-title":"Myosins in cell junctions","volume":"2","author":"Liu","year":"2012","journal-title":"Bioarchitecture"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2251","DOI":"10.1113\/JP275871","article-title":"Initiation and slow propagation of epileptiform activity from ventral to dorsal medial entorhinal cortex is constrained by an inhibitory gradient","volume":"596","author":"Ridler","year":"2018","journal-title":"J. Physiol."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Gaiottino, J., Norgren, N., Dobson, R., Topping, J., Nissim, A., Malaspina, A., Bestwick, J.P., Monsch, A.U., Regeniter, A., and Lindberg, R.L. (2013). Increased neurofilament light chain blood levels in neurodegenerative neurological diseases. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0075091"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"e22363","DOI":"10.1097\/MD.0000000000022363","article-title":"Neurofilament light chain level in traumatic brain injury: A system review and meta-analysis","volume":"99","author":"Gao","year":"2020","journal-title":"Medicine"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"e610","DOI":"10.1212\/WNL.0000000000009983","article-title":"Neurofilament light as a biomarker in traumatic brain injury","volume":"95","author":"Shahim","year":"2020","journal-title":"Neurology"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"761","DOI":"10.1093\/brain\/awaa451","article-title":"Neurofilament light predicts neurological outcome after subarachnoid haemorrhage","volume":"144","author":"Garland","year":"2021","journal-title":"Brain J. Neurol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1016\/j.neuroscience.2018.07.020","article-title":"Immediate and Medium-term Changes in Cortical and Hippocampal Inhibitory Neuronal Populations after Diffuse TBI","volume":"388","author":"Carron","year":"2018","journal-title":"Neuroscience"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1016\/S0306-4522(97)00145-0","article-title":"GABA(A) receptor subunits in the rat hippocampus II: Altered distribution in kainic acid-induced temporal lobe epilepsy","volume":"80","author":"Schwarzer","year":"1997","journal-title":"Neuroscience"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1007\/s12035-019-01753-z","article-title":"The Recovery of GABAergic Function in the Hippocampus CA1 Region After mTBI","volume":"57","author":"Figueiredo","year":"2020","journal-title":"Mol. Neurobiol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.expneurol.2015.07.028","article-title":"GABAergic interneuronal loss and reduced inhibitory synaptic transmission in the hippocampal CA1 region after mild traumatic brain injury","volume":"273","author":"Prager","year":"2015","journal-title":"Exp. Neurol."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"N\u00fa\u00f1ez-Ochoa, M.A., Chipr\u00e9s-Tinajero, G.A., Gonz\u00e1lez-Dom\u00ednguez, N.P., and Medina-Ceja, L. (2021). Causal relationship of CA3 back-projection to the dentate gyrus and its role in CA1 fast ripple generation. BMC Neurosci., 22.","DOI":"10.1186\/s12868-021-00641-4"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1924","DOI":"10.1152\/jn.1997.77.4.1924","article-title":"Differential epilepsy-associated alterations in postsynaptic GABA(A) receptor function in dentate granule and CA1 neurons","volume":"77","author":"Gibbs","year":"1997","journal-title":"J. Neurophysiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"789","DOI":"10.1007\/s40263-013-0097-3","article-title":"Current place of monoamine oxidase inhibitors in the treatment of depression","volume":"27","author":"Shulman","year":"2013","journal-title":"CNS Drugs"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1323","DOI":"10.1016\/j.bbamcr.2010.09.010","article-title":"Monoamine oxidases (MAO) in the pathogenesis of heart failure and ischemia\/reperfusion injury","volume":"1813","author":"Kaludercic","year":"2011","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/j.cbi.2019.03.003","article-title":"Attenuation of the effects of oxidative stress by the MAO-inhibiting antidepressant and carbonyl scavenger phenelzine","volume":"304","author":"Baker","year":"2019","journal-title":"Chem. Biol. Interact."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"795259","DOI":"10.1155\/2012\/795259","article-title":"Oxidative stress and epilepsy: Literature review","volume":"2012","author":"Aguiar","year":"2012","journal-title":"Oxid. Med. Cell. Longev."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1302","DOI":"10.1089\/neu.2016.4624","article-title":"Phenelzine Protects Brain Mitochondrial Function In Vitro and In Vivo following Traumatic Brain Injury by Scavenging the Reactive Carbonyls 4-Hydroxynonenal and Acrolein Leading to Cortical Histological Neuroprotection","volume":"34","author":"Cebak","year":"2017","journal-title":"J. Neurotrauma"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"37","DOI":"10.4088\/JCP.11096su1c.06","article-title":"The use of monoamine oxidase inhibitors in primary care","volume":"73","author":"Culpepper","year":"2012","journal-title":"J. Clin. Psychiatry"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1017\/S1092852919001196","article-title":"Revitalizing monoamine oxidase inhibitors: A call for action","volume":"25","author":"Gillman","year":"2020","journal-title":"CNS Spectr."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1016\/0306-4522(93)90206-U","article-title":"Dopaminergic modulation of pilocarpine-induced motor seizures in the rat: The role of hippocampal D2 receptors","volume":"53","author":"Alam","year":"1993","journal-title":"Neuroscience"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"834","DOI":"10.1111\/j.1471-4159.2004.02355.x","article-title":"Anticonvulsant action of hippocampal dopamine and serotonin is independently mediated by D and 5-HT receptors","volume":"89","author":"Clinckers","year":"2004","journal-title":"J. Neurochem."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1111\/j.1471-4159.2006.04277.x","article-title":"Serotonin and epilepsy","volume":"100","author":"Bagdy","year":"2007","journal-title":"J. Neurochem."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Foreman, B., Lee, H., Okonkwo, D.O., Strong, A.J., Pahl, C., Shutter, L.A., Dreier, J.P., Ngwenya, L.B., and Hartings, J.A. (2022). The Relationship between Seizures and Spreading Depolarizations in Patients with Severe Traumatic Brain Injury. Neurocrit. Care, 1\u201318.","DOI":"10.1007\/s12028-022-01441-2"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"19","DOI":"10.3389\/fneur.2018.00019","article-title":"Understanding Spreading Depression from Headache to Sudden Unexpected Death","volume":"9","author":"Cozzolino","year":"2018","journal-title":"Front. Neurol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1001\/jamaneurol.2019.4476","article-title":"Prognostic Value of Spreading Depolarizations in Patients With Severe Traumatic Brain Injury","volume":"77","author":"Hartings","year":"2020","journal-title":"JAMA Neurol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1002\/cne.10905","article-title":"Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse","volume":"467","author":"Tamamaki","year":"2003","journal-title":"J. Comp. Neurol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1007\/s00429-013-0644-1","article-title":"Loss of hippocampal interneurons and epileptogenesis: A comparison of two animal models of acquired epilepsy","volume":"220","author":"Huusko","year":"2015","journal-title":"Brain Struct. Funct."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/bs.apha.2014.11.005","article-title":"Allosteric ligands and their binding sites define \u03b3-aminobutyric acid (GABA) type A receptor subtypes","volume":"73","author":"Olsen","year":"2015","journal-title":"Adv. Pharmacol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1016\/j.conb.2014.07.025","article-title":"Hippocampal network oscillations\u2014Recent insights from in vitro experiments","volume":"31","author":"Butler","year":"2015","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1016\/S0079-6123(07)63041-6","article-title":"Epileptogenesis in the dentate gyrus: A critical perspective","volume":"163","author":"Dudek","year":"2007","journal-title":"Prog. Brain Res."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"4060","DOI":"10.1021\/acs.jproteome.7b00433","article-title":"Evaluation of FASP, SP3, and iST Protocols for Proteomic Sample Preparation in the Low Microgram Range","volume":"16","author":"Sielaff","year":"2017","journal-title":"J. Proteome Res."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1038\/nmeth.2767","article-title":"Drift time-specific collision energies enable deep-coverage data-independent acquisition proteomics","volume":"11","author":"Distler","year":"2014","journal-title":"Nat. Methods"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"795","DOI":"10.1038\/nprot.2016.042","article-title":"Label-free quantification in ion mobility-enhanced data-independent acquisition proteomics","volume":"11","author":"Distler","year":"2016","journal-title":"Nat. Protoc."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1074\/mcp.M500230-MCP200","article-title":"Absolute quantification of proteins by LCMSE: A virtue of parallel MS acquisition* S","volume":"5","author":"Silva","year":"2006","journal-title":"Mol. Cell. Proteom."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1883","DOI":"10.1089\/neu.2015.4220","article-title":"Underlying Cortical Dysplasia as Risk Factor for Traumatic Epilepsy: An Animal Study","volume":"33","author":"Nemes","year":"2016","journal-title":"J. Neurotrauma"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"107352","DOI":"10.1016\/j.yebeh.2020.107352","article-title":"Posttraumatic epilepsy may be a state in which underlying epileptogenicity involves focal cortical dysplasia","volume":"114","author":"Sakakura","year":"2021","journal-title":"Epilepsy Behav."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/7\/3902\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:47:55Z","timestamp":1760136475000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/7\/3902"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,3,31]]},"references-count":69,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2022,4]]}},"alternative-id":["ijms23073902"],"URL":"https:\/\/doi.org\/10.3390\/ijms23073902","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,3,31]]}}}